Auxin apical dominance governed by the OsAsp1-OsTIF1 complex determines distinctive rice caryopses development on different branches
In rice (Oryza sativa), caryopses located on proximal secondary branches (CSBs) have smaller grain size and poorer grain filling than those located on apical primary branches (CPBs), greatly limiting grain yield. However, the molecular mechanism responsible for developmental differences between CPBs...
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| creator | Chang, Shu Chen, Yixing Jia, Shenghua Li, Yihao Liu, Kun Lin, Zhouhua Wang, Hanmeng Chu, Zhilin Liu, Jin Xi, Chao Zhao, Heping Han, Shengcheng Wang, Yingdian |
| description | In rice (Oryza sativa), caryopses located on proximal secondary branches (CSBs) have smaller grain size and poorer grain filling than those located on apical primary branches (CPBs), greatly limiting grain yield. However, the molecular mechanism responsible for developmental differences between CPBs and CSBs remains elusive. In this transcriptome-wide expression study, we identified the gene Aspartic Protease 1 (OsAsp1), which reaches an earlier and higher transcriptional peak in CPBs than in CSBs after pollination. Disruption of OsAsp1 expression in the heterozygous T-DNA line asp1-1+/-eliminated developmental differences between CPBs and CSBs. OsAsp1 negatively regulated the transcriptional inhibitor of auxin biosynthesis, OsTAA1 transcriptional inhibition factor 1 (OsTIF1), to preserve indole-3-acetic acid (IAA) apical dominance in CPBs and CSBs. IAA also facilitated OsTIF1 translocation from the endoplasmic reticulum (ER) to the nucleus by releasing the interaction of OsTIF1 with OsAsp1 to regulate caryopses IAA levels via a feedback loop. IAA promoted transcription of OsAsp1 through MADS29 to maintain an OsAsp1 differential between CPBs and CSBs during pollination. Together, these findings provide a mechanistic explanation for the distributed auxin differential between CPBs and CSBs to regulate distinct caryopses development in different rice branches and potential targets for engineering yield improvement in crops. |
| doi_str_mv | 10.1371/journal.pgen.1009157 |
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However, the molecular mechanism responsible for developmental differences between CPBs and CSBs remains elusive. In this transcriptome-wide expression study, we identified the gene Aspartic Protease 1 (OsAsp1), which reaches an earlier and higher transcriptional peak in CPBs than in CSBs after pollination. Disruption of OsAsp1 expression in the heterozygous T-DNA line asp1-1+/-eliminated developmental differences between CPBs and CSBs. OsAsp1 negatively regulated the transcriptional inhibitor of auxin biosynthesis, OsTAA1 transcriptional inhibition factor 1 (OsTIF1), to preserve indole-3-acetic acid (IAA) apical dominance in CPBs and CSBs. IAA also facilitated OsTIF1 translocation from the endoplasmic reticulum (ER) to the nucleus by releasing the interaction of OsTIF1 with OsAsp1 to regulate caryopses IAA levels via a feedback loop. IAA promoted transcription of OsAsp1 through MADS29 to maintain an OsAsp1 differential between CPBs and CSBs during pollination. Together, these findings provide a mechanistic explanation for the distributed auxin differential between CPBs and CSBs to regulate distinct caryopses development in different rice branches and potential targets for engineering yield improvement in crops.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1009157</identifier><identifier>PMID: 33108367</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Apical dominance ; Aspartic Acid Proteases - genetics ; Aspartic endopeptidase ; Aspartic proteinases ; Auxin ; Biology and Life Sciences ; Cell growth ; Control ; Dominance ; Edible Grain - genetics ; Edible Grain - growth & development ; Endoplasmic reticulum ; Endoplasmic Reticulum - genetics ; Gene expression ; Gene Expression Regulation, Plant - genetics ; Genetic aspects ; Grain size ; Indoleacetic acid ; Indoleacetic Acids - metabolism ; Laboratories ; Life sciences ; Nuclear Proteins - genetics ; Oryza - genetics ; Oryza - growth & development ; Oryza sativa ; Physiological aspects ; Plant Development - genetics ; Plant Growth Regulators - genetics ; Plant Proteins - genetics ; Pollination ; Pollination - genetics ; Polymerase chain reaction ; Research and Analysis Methods ; Rice ; Seeds ; Software ; T-DNA ; Transcription factors ; Transcription Factors - genetics</subject><ispartof>PLoS genetics, 2020-10, Vol.16 (10), p.e1009157-e1009157</ispartof><rights>COPYRIGHT 2020 Public Library of Science</rights><rights>2020 Chang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2020 Chang et al 2020 Chang et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c726t-9a8879b7276ab588a42fe32bcdd3befe7386b7323ee0982f156630830becab453</citedby><cites>FETCH-LOGICAL-c726t-9a8879b7276ab588a42fe32bcdd3befe7386b7323ee0982f156630830becab453</cites><orcidid>0000-0002-9893-4295 ; 0000-0003-4758-1845 ; 0000-0002-4039-7589</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7647119/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7647119/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33108367$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chang, Shu</creatorcontrib><creatorcontrib>Chen, Yixing</creatorcontrib><creatorcontrib>Jia, Shenghua</creatorcontrib><creatorcontrib>Li, Yihao</creatorcontrib><creatorcontrib>Liu, Kun</creatorcontrib><creatorcontrib>Lin, Zhouhua</creatorcontrib><creatorcontrib>Wang, Hanmeng</creatorcontrib><creatorcontrib>Chu, Zhilin</creatorcontrib><creatorcontrib>Liu, Jin</creatorcontrib><creatorcontrib>Xi, Chao</creatorcontrib><creatorcontrib>Zhao, Heping</creatorcontrib><creatorcontrib>Han, Shengcheng</creatorcontrib><creatorcontrib>Wang, Yingdian</creatorcontrib><title>Auxin apical dominance governed by the OsAsp1-OsTIF1 complex determines distinctive rice caryopses development on different branches</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>In rice (Oryza sativa), caryopses located on proximal secondary branches (CSBs) have smaller grain size and poorer grain filling than those located on apical primary branches (CPBs), greatly limiting grain yield. However, the molecular mechanism responsible for developmental differences between CPBs and CSBs remains elusive. In this transcriptome-wide expression study, we identified the gene Aspartic Protease 1 (OsAsp1), which reaches an earlier and higher transcriptional peak in CPBs than in CSBs after pollination. Disruption of OsAsp1 expression in the heterozygous T-DNA line asp1-1+/-eliminated developmental differences between CPBs and CSBs. OsAsp1 negatively regulated the transcriptional inhibitor of auxin biosynthesis, OsTAA1 transcriptional inhibition factor 1 (OsTIF1), to preserve indole-3-acetic acid (IAA) apical dominance in CPBs and CSBs. IAA also facilitated OsTIF1 translocation from the endoplasmic reticulum (ER) to the nucleus by releasing the interaction of OsTIF1 with OsAsp1 to regulate caryopses IAA levels via a feedback loop. IAA promoted transcription of OsAsp1 through MADS29 to maintain an OsAsp1 differential between CPBs and CSBs during pollination. Together, these findings provide a mechanistic explanation for the distributed auxin differential between CPBs and CSBs to regulate distinct caryopses development in different rice branches and potential targets for engineering yield improvement in crops.</description><subject>Apical dominance</subject><subject>Aspartic Acid Proteases - genetics</subject><subject>Aspartic endopeptidase</subject><subject>Aspartic proteinases</subject><subject>Auxin</subject><subject>Biology and Life Sciences</subject><subject>Cell growth</subject><subject>Control</subject><subject>Dominance</subject><subject>Edible Grain - genetics</subject><subject>Edible Grain - growth & development</subject><subject>Endoplasmic reticulum</subject><subject>Endoplasmic Reticulum - genetics</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant - genetics</subject><subject>Genetic aspects</subject><subject>Grain size</subject><subject>Indoleacetic acid</subject><subject>Indoleacetic Acids - metabolism</subject><subject>Laboratories</subject><subject>Life sciences</subject><subject>Nuclear Proteins - genetics</subject><subject>Oryza - genetics</subject><subject>Oryza - growth & development</subject><subject>Oryza sativa</subject><subject>Physiological aspects</subject><subject>Plant Development - genetics</subject><subject>Plant Growth Regulators - genetics</subject><subject>Plant Proteins - genetics</subject><subject>Pollination</subject><subject>Pollination - genetics</subject><subject>Polymerase chain reaction</subject><subject>Research and Analysis Methods</subject><subject>Rice</subject><subject>Seeds</subject><subject>Software</subject><subject>T-DNA</subject><subject>Transcription factors</subject><subject>Transcription Factors - genetics</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqVk1Fv0zAUhSMEYmPwDxBEQkLw0GLHSZy8IFUTg0oTlWDwajnOdevJsTPbqbp3fjgO7aYG7QGUh8T2d87NudZNkpcYzTGh-MO1HZzhet6vwcwxQjUu6KPkFBcFmdEc5Y-Pvk-SZ95fI0SKqqZPkxNCMKpISU-TX4thp0zKeyW4TlvbKcONgHRtt-AMtGlzm4YNpCu_8D2erfzV8gKnwna9hl3aQgAXJeDTVvmgjAhqC6lT0UFwd2t7Px7BFrTtOzAhtSaSUoIbF42LtTbgnydPJNceXhzeZ8mPi09X519ml6vPy_PF5UzQrAyzmlcVrRua0ZI3RVXxPJNAska0LWlAAiVV2VCSEQBUV5nERVmSmBM1IHiTF-Qseb337bX17NBAz7K8RBjjvMwisdwTreXXrHeqiymY5Yr92bBuzbgLSmhgnEDe1FRKWWQ5zTJeY0AYUVFwiSoM0evjodrQdNCKmNhxPTGdnhi1YbHvjJY5xbiOBu8OBs7eDOAD65QXoDU3YIfxv4sCU4LqMdmbv9CH0x2oNY8BlJE21hWjKVuUsT8El2j0mj9AxaeFTglrQKq4PxG8nwgiE2AX1nzwni2_f_sP9uu_s6ufU_btEbsBrsPGWz0EZY2fgvkeFM5670DeXwhGbBysu86xcbDYYbCi7NXxZd6L7iaJ_AYyaR32</recordid><startdate>20201027</startdate><enddate>20201027</enddate><creator>Chang, Shu</creator><creator>Chen, Yixing</creator><creator>Jia, Shenghua</creator><creator>Li, Yihao</creator><creator>Liu, Kun</creator><creator>Lin, Zhouhua</creator><creator>Wang, Hanmeng</creator><creator>Chu, Zhilin</creator><creator>Liu, Jin</creator><creator>Xi, Chao</creator><creator>Zhao, Heping</creator><creator>Han, Shengcheng</creator><creator>Wang, Yingdian</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-9893-4295</orcidid><orcidid>https://orcid.org/0000-0003-4758-1845</orcidid><orcidid>https://orcid.org/0000-0002-4039-7589</orcidid></search><sort><creationdate>20201027</creationdate><title>Auxin apical dominance governed by the OsAsp1-OsTIF1 complex determines distinctive rice caryopses development on different branches</title><author>Chang, Shu ; Chen, Yixing ; Jia, Shenghua ; Li, Yihao ; Liu, Kun ; Lin, Zhouhua ; Wang, Hanmeng ; Chu, Zhilin ; Liu, Jin ; Xi, Chao ; Zhao, Heping ; Han, Shengcheng ; Wang, Yingdian</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c726t-9a8879b7276ab588a42fe32bcdd3befe7386b7323ee0982f156630830becab453</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Apical dominance</topic><topic>Aspartic Acid Proteases - 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genetics</topic><topic>Polymerase chain reaction</topic><topic>Research and Analysis Methods</topic><topic>Rice</topic><topic>Seeds</topic><topic>Software</topic><topic>T-DNA</topic><topic>Transcription factors</topic><topic>Transcription Factors - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Chang, Shu</creatorcontrib><creatorcontrib>Chen, Yixing</creatorcontrib><creatorcontrib>Jia, Shenghua</creatorcontrib><creatorcontrib>Li, Yihao</creatorcontrib><creatorcontrib>Liu, Kun</creatorcontrib><creatorcontrib>Lin, Zhouhua</creatorcontrib><creatorcontrib>Wang, Hanmeng</creatorcontrib><creatorcontrib>Chu, Zhilin</creatorcontrib><creatorcontrib>Liu, Jin</creatorcontrib><creatorcontrib>Xi, Chao</creatorcontrib><creatorcontrib>Zhao, Heping</creatorcontrib><creatorcontrib>Han, Shengcheng</creatorcontrib><creatorcontrib>Wang, Yingdian</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Chang, Shu</au><au>Chen, Yixing</au><au>Jia, Shenghua</au><au>Li, Yihao</au><au>Liu, Kun</au><au>Lin, Zhouhua</au><au>Wang, Hanmeng</au><au>Chu, Zhilin</au><au>Liu, Jin</au><au>Xi, Chao</au><au>Zhao, Heping</au><au>Han, Shengcheng</au><au>Wang, Yingdian</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Auxin apical dominance governed by the OsAsp1-OsTIF1 complex determines distinctive rice caryopses development on different branches</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2020-10-27</date><risdate>2020</risdate><volume>16</volume><issue>10</issue><spage>e1009157</spage><epage>e1009157</epage><pages>e1009157-e1009157</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>In rice (Oryza sativa), caryopses located on proximal secondary branches (CSBs) have smaller grain size and poorer grain filling than those located on apical primary branches (CPBs), greatly limiting grain yield. However, the molecular mechanism responsible for developmental differences between CPBs and CSBs remains elusive. In this transcriptome-wide expression study, we identified the gene Aspartic Protease 1 (OsAsp1), which reaches an earlier and higher transcriptional peak in CPBs than in CSBs after pollination. Disruption of OsAsp1 expression in the heterozygous T-DNA line asp1-1+/-eliminated developmental differences between CPBs and CSBs. OsAsp1 negatively regulated the transcriptional inhibitor of auxin biosynthesis, OsTAA1 transcriptional inhibition factor 1 (OsTIF1), to preserve indole-3-acetic acid (IAA) apical dominance in CPBs and CSBs. IAA also facilitated OsTIF1 translocation from the endoplasmic reticulum (ER) to the nucleus by releasing the interaction of OsTIF1 with OsAsp1 to regulate caryopses IAA levels via a feedback loop. IAA promoted transcription of OsAsp1 through MADS29 to maintain an OsAsp1 differential between CPBs and CSBs during pollination. Together, these findings provide a mechanistic explanation for the distributed auxin differential between CPBs and CSBs to regulate distinct caryopses development in different rice branches and potential targets for engineering yield improvement in crops.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>33108367</pmid><doi>10.1371/journal.pgen.1009157</doi><orcidid>https://orcid.org/0000-0002-9893-4295</orcidid><orcidid>https://orcid.org/0000-0003-4758-1845</orcidid><orcidid>https://orcid.org/0000-0002-4039-7589</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Apical dominance Aspartic Acid Proteases - genetics Aspartic endopeptidase Aspartic proteinases Auxin Biology and Life Sciences Cell growth Control Dominance Edible Grain - genetics Edible Grain - growth & development Endoplasmic reticulum Endoplasmic Reticulum - genetics Gene expression Gene Expression Regulation, Plant - genetics Genetic aspects Grain size Indoleacetic acid Indoleacetic Acids - metabolism Laboratories Life sciences Nuclear Proteins - genetics Oryza - genetics Oryza - growth & development Oryza sativa Physiological aspects Plant Development - genetics Plant Growth Regulators - genetics Plant Proteins - genetics Pollination Pollination - genetics Polymerase chain reaction Research and Analysis Methods Rice Seeds Software T-DNA Transcription factors Transcription Factors - genetics |
| title | Auxin apical dominance governed by the OsAsp1-OsTIF1 complex determines distinctive rice caryopses development on different branches |
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